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Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3

Abstract

Centromeres can arise de novo from non-centromeric regions, which are often called “neocentromeres.” Neocentromere formation provides the best evidence for the concept that centromere function is not determined by the underlying DNA sequences, but controlled by poorly understood epigenetic mechanisms. Numerous neocentromeres have been reported in several plant and animal species. However, it has been elusive how and why a specific chromosomal region is chosen to be a new centromere during the neocentromere activation events. We report recurrent establishment of neocentromeres in a pericentromeric region of chromosome 3 in maize (Zea mays). This latent region is located in the short arm and is only 2 Mb away from the centromere (Cen3) of chromosome 3. At least three independent neocentromere activation events, which were likely induced by different mechanisms, occurred within this latent region. We mapped the binding domains of CENH3, the centromere-specific H3 histone variant, of the three neocentromeres and analyzed the genomic and epigenomic features associated with Cen3, the de novo centromeres and an inactivated centromere derived from an ancestral chromosome. Our results indicate that lack of genes and transcription and a relatively high level of DNA methylation in this pericentromeric region may provide a favorable chromatin environment for neocentromere activation.

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Abbreviations

ChIP:

Chromatin immunoprecipitation

DAPI:

4′,6-diamidino-2-phenylindole

FISH:

Flourescence in situ hybridization

OMA:

Oat-maize chromosome addition

SNP:

Single nucleotide polymorphism

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Acknowledgements

We thank Dr. Patrick Schnable for providing the seeds of maize line ax-3 and Drs. Kelly Dawe and Jonathan Gent for valuable comments on the manuscript. This work was supported by the National Science Foundation (NSF) grant 1338897 to B.S.G. and NSF grant IOS-1444514 to J.A.B. and J.J.

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Contributions

H.Z and J.J. designed the research, Z.Z. and D.H.K. performed experiments, H.Z., J.A.B., and J.J. analyzed data, and H.Z., B.S.G., J.A.B., and J.J. wrote the article.

Corresponding authors

Correspondence to James A. Birchler or Jiming Jiang.

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Responsible Editor: Hans de Jong

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Zhao, H., Zeng, Z., Koo, DH. et al. Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3. Chromosome Res 25, 299–311 (2017). https://doi.org/10.1007/s10577-017-9564-x

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  • DOI: https://doi.org/10.1007/s10577-017-9564-x

Keywords

  • Centromere
  • CENH3
  • neocentromere
  • centromeric genes
  • centromeric chromatin